Biology subjects

Bee, M. A.

Publications and source records attributed to Bee, M. A..

10 recordsLinked to original sources

bioRxiv2025

Treefrogs exploit temporal onset synchrony and harmonicity in forming auditory objects of vocal communication signals

Animals frequently communicate in dense social aggregations characterized by the presence of overlapping signals from multiple individuals. Receivers have to perceptually organize these overlapping signals into distinct auditory objects, each corresponding to the perceptual representation of an individual signal. All the signal components produced by the same individual should be integrated into a unitary auditory object while those produced by distinct individuals should be segregated. The principles of auditory object formation and their importance in vocal communication are less understood in non-human animals relative to humans. Here, using American green treefrogs, Hyla cinerea, we tested the hypothesis that receivers exploit the relative timing and harmonic relatedness of multiple spectral components to integrate or segregate sounds during auditory object formation. Using phonotaxis as a behavioral assay, females were given a choice between an attractive conspecific call consisting of three spectral components and a composite call consisting of the same three conspecific spectral components to which we added three spectral components from the call of a heterospecific sister species (Hyla gratiosa). The addition of heterospecific components to conspecific calls renders them less attractive. Across treatments, we manipulated the relative onset timing and harmonic relatedness of the heterospecific components in relation to the conspecific components. We predicted that asynchronous temporal onsets and inharmonic relationships between the conspecific and heterospecific components would promote their perceptual segregation. Our findings are consistent with this prediction. We discuss these findings in the light of parallel perceptual processes across animal taxa and neuroethological theories of auditory processing.

neuroscience↗

bioRxiv2023

Perceptual salience is insufficient for auditory streaming in eastern gray treefrogs ( Hyla versicolor )

Auditory streaming underlies a receivers ability to organize complex mixtures of auditory input into distinct perceptual "streams" that represent different sound sources in the environment. During auditory streaming, sounds produced by the same source are integrated through time into a single, coherent auditory stream that is perceptually segregated from other concurrent sounds. Based on human psychoacoustic studies, a prominent hypothesis regarding auditory streaming is that any perceptually salient acoustic difference between sounds can promote their segregation into distinct auditory streams. Here, we used the eastern gray treefrog, Hyla versicolor, to test this hypothesis in the context of vocal communication in a non-human animal. In this system, females choose their mate based on perceiving features of a males pulsatile advertisement calls in social environments (choruses) characterized by mixtures of overlapping vocalizations. We employed an experimental paradigm from human psychoacoustics to design interleaved pulsatile sequences (ABAB...) that mimicked key features of the species advertisement call, and in which alternating pulses differed in pulse rise time, which is a robust species recognition cue in eastern gray treefrogs. Using phonotaxis assays, we found no evidence that perceptually salient differences in pulse rise time promoted the segregation of interleaved pulse sequences into distinct auditory streams. These results suggest the hypothesis that any perceptually salient acoustic difference can be exploited as a cue for stream segregation is not supported in all species. We discuss these findings in the context of cues used for species recognition and auditory streaming.

animal behavior and cognition↗

bioRxiv2022

Informational Masking Can Constrain Acoustically Guided Mating Behavior

Animals often communicate acoustically in noisy social environments, yet how receivers extract relevant information from overlapping sounds is poorly understood. Studies of animal communication in noise are typically based on a traditional filterbank model of hearing focused on energetic masking, where spectrotemporal overlap in peripheral auditory filters limits signal audibility. By contrast, studies of human speech show that background sounds can also interfere with selecting and attending to otherwise audible signals in a phenomenon known as informational masking. Whether informational masking constrains acoustic communication in nonhuman animals remains poorly understood. Through controlled laboratory experiments with treefrogs (Hyla chrysoscelis), we demonstrate, for the first time in a nonhuman animal, that informational masking can impair crucial mate-choice decisions when vocal signals and other concurrent sounds share similar temporal features. These impacts spanned a wide range of signal-to-noise ratios, occurred in the absence of spectrotemporal overlap in the auditory periphery, and were strongest when interfering sounds fell within a frequency band salient for vocal processing. Our findings challenge conventional views on how noise impacts animal communication by establishing informational masking as a general communication problem shared by humans and other animals. These results highlight the need to distinguish between energetic and informational masking to understand the evolution of signaling in complex acoustic environments.

neuroscience↗

bioRxiv2021

Neural Basis of Acoustic Species Recognition in a Cryptic Species Complex

Sexual traits that promote species recognition are important drivers of reproductive isolation, especially among closely related species. Identifying neural processes that shape species differences in recognition is crucial for understanding the causal mechanisms of reproductive isolation. Temporal patterns are salient features of sexual signals that are widely used in species recognition by several taxa, including anurans. Recent advances in our understanding of temporal processing by the anuran auditory system provide an excellent opportunity to investigate the neural basis of species-specific recognition. The anuran inferior colliculus (IC) consists of neurons that are selective for temporal features of calls. Of potential relevance are auditory neurons known as interval-counting neurons (ICNs) that are often selective for the pulse rate of conspecific advertisement calls. Here, we took advantage of a species differences in temporal selectivity for pulsatile advertisement calls exhibited by two cryptic species of gray treefrog (Hyla chrysoscelis and Hyla versicolor) to test the hypothesis that ICNs mediate acoustic species recognition. We tested this hypothesis by examining the extent to which the threshold number of pulses required to elicit behavioral responses from females and neural responses from ICNs was similar within each species but potentially different between the two species. In support of our hypothesis, we found that a species difference in behavioral pulse number thresholds corresponded closely to a parallel species difference in neural pulse number thresholds. However, this relationship held only for ICNs that exhibited band-pass tuning for conspecific pulse rates. Together, these findings suggest that differences in temporal processing of a subset of ICNs provide a mechanistic explanation for reproductive isolation between two cryptic and syntopically breeding treefrog species. Summary StatementTemporal processing by a subset of midbrain auditory neurons plays key roles in decoding information about species identity in anurans.

evolutionary biology↗

bioRxiv2021

Predicting and measuring decision rules for social recognition in a Neotropical frog

Many animals use signals, such as vocalizations, to recognize familiar individuals. However, animals risk making recognition mistakes because the signal properties of different individuals often overlap due to within-individual variation in signal production. To understand the relationship between signal variation and decision rules for social recognition, we studied male golden rocket frogs, which recognize the calls of territory neighbors and respond less aggressively to a neighbors calls than to the calls of strangers. We quantified patterns of individual variation in acoustic properties of calls and predicted optimal discrimination thresholds using a signal detection theory model of receiver utility that incorporated signal variation, the payoffs of correct and incorrect decisions, and the rates of encounters with neighbors and strangers. We then experimentally determined thresholds for discriminating between neighbors and strangers using a habituation-discrimination experiment with territorial males in the field. Males required a threshold difference between 9% and 12% to discriminate between calls differing in temporal properties; this threshold matched those predicted by a signal detection theory model under ecologically realistic assumptions of infrequent encounters with strangers and relatively costly missed detections of strangers. We demonstrate empirically that receivers group continuous variation in vocalizations into discrete social categories and show that signal detection theory can be applied to investigate evolved decision rules.

animal behavior and cognition↗

bioRxiv2021

Identity signaling, identity reception and the evolution of social recognition in a Neotropical frog

Animals recognize familiar individuals to perform a variety of important social behaviors. Social recognition is often mediated by communication between signalers who produce signals that contain identity information and receivers who categorize these signals based on previous experience. We tested two hypotheses about adaptations in signalers and receivers that enable the evolution of social recognition using two species of closely related territorial poison frogs. Male golden rocket frogs (Anomaloglossus beebei) recognize the advertisement calls of conspecific territory neighbors and display a "dear enemy effect" by responding less aggressively to neighbors than strangers, while male Kai rocket frogs (A. kaiei) do not. Our results did not support the identity signaling hypothesis: both species produced advertisement calls that contain similar amounts of identity information. Our results did support the identity reception hypothesis: both species exhibited habituation of aggression to playbacks simulating the arrival of a new neighbor, but only golden rocket frogs showed renewed aggression when they subsequently heard calls from a different male. These results suggest that an ancestral mechanism of plasticity in aggression common among frogs has been modified through natural selection to be specific to calls of individual males in golden rocket frogs, enabling a social recognition system.

animal behavior and cognition↗

bioRxiv2021

Convergent evolution of a novel blood-red nectar pigment in vertebrate-pollinated flowers

Nesocodon mauritianus (Campanulaceae) produces a blood-red nectar that has been proposed to serve as a visual attractant for pollinator visitation. Here we show that the nectars red color is derived from a novel alkaloid termed nesocodin. The first nectar produced is acidic and pale yellow in color, but slowly becomes alkaline before taking on its characteristic red color. Three enzymes secreted into the nectar are either necessary or sufficient for pigment production, including (1) a carbonic anhydrase that creates an alkaline environment, (2) an aryl alcohol oxidase that generates sinapaldehyde, a pigment precursor, and (3) a ferritin-like catalase that protects nesocodin from degradation by hydrogen peroxide. Our findings demonstrate how these three enzymatic activities allow for the condensation of sinapaldehyde and proline to form a novel pigment with a stable imine bond, which in turn is attractive to Phelsuma geckos, the presumed pollinators of Nesocodon. We also identify nesocodin in the red nectar of the distantly related Jaltomata herrerae and provide evidence for convergent evolution of this trait. While the overall enzymatic activities required for red pigment formation in both Nesocodon and J. herrerae nectars are identical, the associated genes encoding the enzymes are not orthologous and, in the case of the aryl alcohol oxidase, even belong to different protein families. This work cumulatively identifies a novel, convergently evolved trait in two vertebrate-pollinated species, suggesting the red pigment is selectively favored and that only a limited number of compounds are likely to underlie this adaptation. SignificanceNearly 90% of flowering plants produce nectar to attract pollinators. Beyond sugars, many types of nectar solutes play important ecological roles; however, the molecular basis for the diversity of nectar composition across species is less explored. One rare trait among flowering plants is the production of colored nectar, which may function to attract and guide prospective pollinators. Our findings indicate convergent evolution of a red-colored nectar across two distantly related plant species. Behavioral data show that the red pigment attracts diurnal geckos, a presumed pollinator of one of these plants. These findings join a growing list of examples of distinct biochemical and molecular mechanisms underlying evolutionary convergence, and provide a fascinating system for testing how interactions across species drive the evolution of novel pigments in an understudied context.

evolutionary biology↗

bioRxiv2020

Lung-to-ear sound transmission does not improve directional hearing in green treefrogs (Hyla cinerea)

Amphibians are unique among extant vertebrates in having middle ear cavities that are internally coupled to each other and to the lungs. In frogs, the lung-to-ear sound transmission pathway can influence the tympanums inherent directionality, but what role such effects might play in directional hearing remain unclear. In this study of the American green treefrog (Hyla cinerea), we tested the hypothesis that the lung-to-ear sound transmission pathway functions to improve directional hearing, particularly in the context of interspecific sexual communication. Using laser vibrometry, we measured the tympanums vibration amplitude in females in response to a frequency modulated sweep presented from 12 sound incidence angles in azimuth. Tympanum directionality was determined across three states of lung inflation (inflated, deflated, reinflated) both for a single tympanum in the form of the vibration amplitude difference (VAD) and for binaural comparisons in the form of the interaural vibration amplitude difference (IVAD). The state of lung inflation had negligible effects (typically less than 0.5 dB) on both VADs and IVADs at frequencies emphasized in the advertisement calls produced by conspecific males (834 Hz and 2730 Hz). Directionality at the peak resonance frequency of the lungs (1558 Hz) was improved by {cong} 3 dB for a single tympanum when the lungs were inflated versus deflated, but IVADs were not impacted by the state of lung inflation. Based on these results, we reject the hypothesis that the lung-to-ear sound transmission pathway functions to improve directional hearing in frogs. SUMMARY STATEMENTContrary to prevailing views on the mechanisms of hearing in frogs, the lung-to-ear pathway for sound transmission does not improve directional hearing in these vociferous vertebrates.

zoology↗

bioRxiv2020

Lungs contribute to solving the frog's cocktail party problem by enhancing the spectral contrast of conspecific vocal signals

Noise impairs signal perception and is a major source of selection on animal communication. Identifying adaptations that enable receivers to cope with noise is critical to discovering how animal sensory and communication systems evolve. We integrated biophysical and bioacoustic measurements with physiological modeling to demonstrate that the lungs of frogs serve a heretofore unknown noise-control function in vocal communication. Lung resonance enhances the signal-to-noise ratio for communication by selectively reducing the tympanums sensitivity at critical frequencies where the tuning of two inner ear organs overlaps. Social network analysis of citizen-science data on frog calling behavior indicates the calls of other frog species in multi-species choruses are a prominent source of environmental noise attenuated by the lungs. These data reveal that an ancient adaptation for detecting sound via the lungs has been evolutionarily co-opted to create spectral contrast enhancement that contributes to solving a multi-species cocktail party problem.

zoology↗

bioRxiv2020

Ecological and social drivers of neighbor recognition and the dear enemy effect in a poison frog

Navigating social relationships frequently rests on the ability to recognize familiar individuals using phenotypic characteristics. Across diverse taxa, animals vary in their capacities for social recognition but the ecological and social sources of selection for recognition are often unclear. In a comparative study of two closely related species of poison frogs, we identified a species difference in social recognition of territory neighbors and investigated potential sources of selection underlying this difference. In response to acoustic playbacks, male golden rocket frogs (Anomaloglossus beebei) recognized the calls of neighbors and displayed a "dear enemy effect" by responding less aggressively to neighbors calls than strangers calls. In contrast, male Kai rocket frogs (Anomaloglossus kaiei) were equally aggressive to the calls of neighbors and strangers. This species difference in behavior was associated with key differences in reproductive ecology and characteristics of territories. Golden rocket frogs defended reproductive resources in the form of bromeliads, which is expected to create a threat asymmetry between neighbors and strangers favoring decreased aggression to neighbors. In contrast, Kai rocket frogs did not defend reproductive resources. Further, compared with Kai rocket frog territories, golden rocket frog territories occurred at higher densities and were defended for longer periods of time, creating a more complex social environment with more opportunities for repeated but unnecessary aggression between neighbors, which should favor the ability to recognize and exhibit less aggression towards neighbors. These results suggest that differences in reproductive ecology can drive changes in social structure that select for social recognition.

animal behavior and cognition↗